Populations Of Prairie Voles Research Articles

Influence of genetic similarity and social setting on extra-pair parentage in prairie voles

Abstract Social monogamy is rare in mammals, but in those species in which it occurs, individuals frequently engage in extra-pair copulation (EPC). Numerous hypotheses have been proposed to explain EPC, but relatively few field studies have examined factors influencing EPC in socially monogamous mammals. Prairie voles (Microtus ochrogaster) are a socially monogamous rodent in which extra-pair paternity (EPP) is common. Using genetic data from a 3-year study of a natural population of prairie voles, we investigated whether the negative consequences of inbreeding and the structure of social units (male–female pairs vs. groups; adult sex ratio within groups) were factors affecting EPC. We found strong evidence that genetic similarity between males and females that produced offspring via EPC was less than that between social partners, as would be expected if avoiding inbreeding depression influenced the occurrence of EPC. Social unit structure was also a factor involved with extra-pair parentage. Contrary to our expectations, the greater the proportion of females in the group, the lower the chance of EPC resulting in offspring production by females, and, similarly, the chance of EPP by males declined as the proportion of males within the group increased. However, neither males nor females were more likely to produce offspring from EPC when they were living in pairs versus groups. One implication of these results is that EPC may be influenced more by female behaviors, such as mate choice, than male mate guarding. Overall, our results suggest that the proximate factors influencing EPC in prairie voles are complex but include the cost of inbreeding depression and the structure of social units.

Functional Connectivity Differences Between Two Culturally Distinct Prairie Vole Populations: Insights Into the Prosocial Network

BackgroundThe goal of this study was to elucidate the fundamental connectivity—resting-state connectivity—within and between nodes in the olfactory and prosocial (PS) cores, which permits the expression of social monogamy in males; and how differential connectivity accounts for differential expression of prosociality and aggression. MethodsUsing resting-state functional magnetic resonance imaging, we integrated graph theory analysis to compare functional connectivity between two culturally/behaviorally distinct male prairie voles (Microtusochrogaster). ResultsIllinois males display significantly higher levels of prosocial behavior and lower levels of aggression than KI (Kansas dam and Illinois sire) males, which are associated with differences in underlying neural mechanisms and brain microarchitecture. Shared connectivity 1) between the anterior hypothalamic area and the paraventricular nucleus and 2) between the medial preoptic area and bed nucleus of the stria terminalis and the nucleus accumbens core suggests essential relationships required for male prosocial behavior. In contrast, Illinois males displayed higher levels of global connectivity and PS intracore connectivity, a greater role for the bed nucleus of the stria terminalis and anterior hypothalamic area, which were degree connectivity hubs, and greater PS and olfactory intercore connectivity. ConclusionsThese findings suggest that behavioral differences are associated with PS core degree of connectivity and postsignal induction. This transgenerational system may serve as powerful mental health and drug abuse translational model in future studies.

Medial amygdala ERα expression influences monogamous behaviour of male prairie voles in the field.

Formation of long-term pair-bonds is a complex process, involving multiple neural circuits and is context- and experience-dependent. While laboratory studies using prairie voles have identified the involvement of several neural mechanisms, efforts to translate these findings into predictable field outcomes have been inconsistent at best. Here we test the hypothesis that inhibition of oestrogen receptor alpha (ERα) in the medial amygdala of male prairie voles would significantly increase the expression of social monogamy in the field. Prairie vole populations of equal sex ratio were established in outdoor enclosures with males bred for high levels of ERα expression and low levels of prosocial behaviour associated with social monogamy. Medial amygdala ERα expression was knocked down in half the males per population. Knockdown males displayed a greater degree of social monogamy in five of the eight behavioural indices assessed. This study demonstrates the robust nature of ERα in playing a critical role in the expression of male social monogamy in a field setting.

Breeding patterns of female prairie voles (Microtus ochrogaster) displaying alternative reproductive tactics.

Individuals of either sex may display alternative behaviors to obtain copulations, but few studies have examined the breeding patterns of females and males in populations where individuals of both sexes exhibit alternative reproductive tactics (ARTs). In prairie voles (Microtus ochrogaster), most adults are territorial, residing at a single nest site either as male-female pairs or as solitary individuals. However, some adults adopt nonterritorial, wandering tactics. During two field seasons monitoring prairie vole populations maintained in seminatural enclosures, we found evidence that females exhibiting different ARTs bred differentially with resident and wandering males. Females residing at a nest with a male bred significantly more often with a paired resident male, primarily their social partner, and significantly less often with male wanderers compared to single resident females or wandering females. These patterns were not due to chance, because paired resident females produced offspring with paired resident males significantly more than expected based on the relative abundance of these males in the population, whereas single resident females produced offspring with male wanderers significantly more than expected based on the proportion of male wanderers in the population. We did not find any evidence that multiple paternity was greater in the litters of single resident females and wanderer females even though these females lacked a male social partner to limit mating access by multiple males. This suggests that mate guarding by a female's male social partner was not the primary determinant of multiple paternity in the litters of females exhibiting different reproductive tactics. However, male ART did affect the likelihood of multiple paternity. Females that produced offspring with single resident or wanderer males had an increased likelihood of multiple paternity relative to females producing offspring with paired resident males. The results of this study show that female and male ARTs can affect breeding patterns.

Maternal and paternal origin differentially affect prosocial behavior and neural mechanisms in prairie voles

This study tested the hypotheses that maternal and paternal effects differentially influence expression of their offspring's adult behavior and underlying neural mechanisms. We predicted that maternal influences would be greater than paternal influences on male offspring. We tested these hypotheses by cross-breeding two phenotypically-, behaviorally- and neuroanatomically-distinct populations of prairie voles (Microtus ochrogaster) from Illinois, which are highly prosocial, and Kansas, which are significantly less prosocial. Females from each population were crossed with males from the other population. F1 crosses were tested as adults to determine the effect of parentage on the expression of prosocial behavior and aggression, using a same-sex dyadic encounter and a heterosexual partner preference test, and for the expression of oxytocin (OT) and arginine vasopressin (AVP) in the paraventricular nucleus of the hypothalamus (PVN). As predicted, all significant differences in males, behavioral, OT and AVP immunoreactivity, were associated exclusively with maternal influences. There was a significant effect of treatment in the OT immunoreactivity of females. The effect of treatment in females’ OT was associated with an interaction of population and sex, while same-sex social interactions differences were associated with population. Finally, in females, paternity influenced heterosexual bonds, with females with Illinois sires forming a partner preference. The results indicate that maternal influences dominate in male offspring, suggesting a parent-of-origin effect, while paternal effects are limited to selected prosocial behavioral expression in daughters.

Dispatches from the field: sociality and reproductive success in prairie voles

One way to characterize sociality is by the type and variability of social organization exhibited by individuals within populations. Social unit size and composition can result in costs and benefits to female group members, which may affect their reproductive success. We tested this hypothesis using data from two natural populations of prairie voles, Microtus ochrogaster , that live in habitats differing in the distribution of vegetation and in population density. During short-term investigations of populations in Indiana and Kansas (4–8 weeks), we detected significant differences between populations in the type of social units in which adult females resided, with most adult females in Kansas living as single females, whereas in Indiana most females resided in groups. However, neither social unit size nor composition was related to female reproductive success in either population. When we studied the same Indiana population for 15 weeks, the length of time that females were detected on the study grid or were residents at a nest predicted the number of offspring they produced. In addition, the number of offspring produced by females tended to decrease with group size, although this relationship was not statistically significant. Finally, social unit size was not significantly related to the amount of time females were detected in the population. Our results suggest that females do not obtain increased direct or indirect fitness by living in larger groups. Rather, persistence and residency status of females in the population are the best predictors of female reproductive success.

Effects of avpr1a length polymorphism on male social behavior and reproduction in semi‐natural populations of prairie voles (Microtus ochrogaster)

AbstractIntraspecific variation in sociosexual behavior has typically been investigated in the context of its relationship with environmental factors, but neurogenetic factors can also influence sociosexual behavior. In laboratory studies of prairie voles (Microtus ochrogaster), length polymorphism of microsatellite DNA within the gene (avpr1a) encoding the vasopressin 1a receptor is correlated with variation in male sociosexual behavior. However, field studies of prairie voles have found the relationship between male avpr1a microsatellite allele length and sociosexual behavior to be more ambiguous, possibly because most males had alleles of intermediate length. We tested the hypothesis that avpr1a microsatellite allele length mediates male sociosexual behavior in field settings by releasing voles into field enclosures where every male possessed two avpr1a microsatellite alleles at least one standard error longer or shorter than the mean length in their population of origin. Voles from an Illinois and Kansas population were examined separately as social monogamy appears more prevalent in the Illinois population. Illinois males with long avpr1a microsatellite alleles had smaller home ranges and overlapped a greater proportion of the home range of the female that they overlapped the most. Kansas males showed the opposite pattern. Illinois, but not Kansas, males with long avpr1a microsatellite alleles sired offspring with more females and sired more litters. Our results support the hypothesis that genetic variation associated with the avpr1a gene plays a role in mediating male prairie vole sociosexual behavior in nature. However, the relationship between specific male behaviors and male avpr1a microsatellite allele length sometimes differed significantly between Kansas and Illinois voles, suggesting relationships between specific male sociosexual behaviors and polymorphism associated with the avpr1a locus are complex, possibly involving specific nucleotide sequences or other population‐specific genetic differences.

Trait-demography relationships underlying small mammal population fluctuations.

Large-scale fluctuations in abundance are a common feature of small mammal populations and have been the subject of extensive research. These demographic fluctuations are often associated with concurrent changes in the average body mass of individuals, sometimes referred to as the 'Chitty effect'. Despite the long-standing recognition of this phenomenon, an empirical investigation of the underlying coupled dynamics of body mass and population growth has been lacking. Using long-term life-history data combined with a trait-based demographic approach, we examined the relationship between body mass and demography in a small mammal population that exhibits non-cyclic, large-scale fluctuations in abundance. We used data from the male segment of a 25-year study of the monogamous prairie vole, Microtus ochrogaster, in Illinois, USA. Specifically, we investigated how trait-demography relationships and trait distributions changed between different phases of population fluctuations, and the consequences of these changes for both trait and population dynamics. We observed phase-specific changes in male adult body mass distribution in this population of prairie voles. Our analyses revealed that these changes were driven by variation in ontogenetic growth, rather than selection acting on the trait. The resulting changes in body mass influenced most life-history processes, and these effects varied among phases of population fluctuation. However, these changes did not propagate to affect the population growth rate due to the small effect of body mass on vital rates, compared to the overall differences in vital rates between phases. The increase phase of the fluctuations was initiated by enhanced survival, particularly of juveniles and fecundity, whereas the decline phase was driven by an overall reduction in fecundity, survival and maturation rates. Our study provides empirical support, as well as a potential mechanism, underlying the observed trait changes accompanying population fluctuations. Body size dynamics and population fluctuations resulted from different life-history processes. Therefore, we conclude that body size dynamics in our population do not drive the observed population dynamics. This more in-depth understanding of different components of small mammal population fluctuations will help us to better identify the mechanistic drivers of this interesting phenomenon.

Spontaneous emergence of overgrown molar teeth in a colony of Prairie voles (Microtus ochrogaster).

Continuously growing incisors are common to all rodents, which include the Microtus genus of voles. However, unlike many rodents, voles also possess continuously growing molars. Here, we report spontaneous molar defects in a population of Prairie voles (Microtus ochrogaster). We identified bilateral protuberances on the ventral surface of the mandible in several voles in our colony. In some cases, the protuberances broke through the cortical bone. The mandibular molars became exposed and infected, and the maxillary molars entered the cranial vault. Visualisation upon soft tissue removal and microcomputed tomography (microCT) analyses confirmed that the protuberances were caused by the overgrowth of the apical ends of the molar teeth. We speculate that the unrestricted growth of the molars was due to the misregulation of the molar dental stem cell niche. Further study of this molar phenotype may yield additional insight into stem cell regulation and the evolution and development of continuously growing teeth.

Length polymorphism at the avpr1a locus is correlated with male reproductive behavior in a natural population of prairie voles (Microtus ochrogaster)

Laboratory studies have shown that vasopressin can influence sociosexual behavior through its action on the vasopressin 1a receptor (V1aR). There is substantial evidence that the length of a microsatellite in the gene (avpr1a) encoding for the V1aR can affect social attachment to females and paternal behavior in male prairie voles under laboratory conditions. However, previous field studies of prairie voles have failed to detect a strong effect of the length of a male’s avpr1a allele on their sociosexual behavior, but these studies are typically much shorter than the average prairie vole breeding lifespan. We examined the relationship between male avpr1a microsatellite allele length and sociosexual behavior in a natural population of prairie voles for 15 weeks, closer to the lifespan of prairie voles in nature. Contrary to predictions, we found that males with the longest avpr1a microsatellite alleles were significantly more likely to sire offspring with more than one female and to sire offspring that survived until trappable age than males with the shortest avpr1a microsatellite allele lengths. This relationship was the strongest for males with the longest tenure on the study site. As in previous field studies, we did not find evidence of a relationship between a male’s avpr1a genotype and any index of social behavior including male residency status or the number of females with which males associate. This is the first study to support the hypothesis that a male’s avpr1a genotype is a factor underlying variation in the genetic mating system of prairie voles under natural conditions.

Are body mass and parasite load related to social partnerships and mating inMicrotus ochrogaster?

Abstract Within socially monogamous species, a male's reproductive success depends on his success at obtaining a social partner with which he mates, as well as gaining extra-pair matings. We investigated the impacts of body mass and parasitism on 2 measures of a male's success at obtaining a social partner (number of female social associations and relative strength of a social bond to a single female) and 2 measures of reproduction (number of females with which a male sires offspring and the number of offspring sired) in natural populations of prairie voles (Microtus ochrogaster) located in Kansas and Indiana. Kansas males with greater endoparasite loads were less likely to have one social partner. Instead, they associated with multiple females although they did not sire offspring with more females than males with lower levels of endoparasitism. We did not find any relationship between endoparasite infestation and the number of females with which males associated in Indiana. There was no association betwe...

Intraspecific variability in the social and genetic mating systems of prairie voles, Microtus ochrogaster

Intraspecific variability in mating systems has been documented previously, but there are few studies where investigators have used intraspecific comparisons to investigate the influence of ecological or demographic factors on social and genetic mating systems. We studied two populations of prairie voles, Microtus ochrogaster, one near Lawrence, Kansas, U.S.A., and the other in Bloomington, Indiana, U.S.A. We examined differences in spatial structuring of vegetation between sites, which might contribute to intraspecific variation in social and genetic mating patterns. Since space use is often related to the mating system, we calculated home range size of a subset of adult males and females in both populations and used live trapping to examine the number of same- or opposite-sex conspecifics sharing capture locations. We applied social network analysis to live-trapping data to quantify the number and strength of social ties with opposite-sex conspecifics. Genetic parentage analysis provided an estimate of the number of mates per individual. We found that space use and overlap with members of the same and opposite sex were best explained by effects of site and sex. The relative strength of social associations with opposite-sex conspecifics was best predicted by site, density and sex. The genetic mating system was best explained by population density. Although we cannot disentangle population density from ecological variables related to site (e.g. distribution of vegetation) that may have affected social monogamy in our study populations, our study shows that extrinsic variables do affect differences in social and genetic mating systems between populations.

Multiple Captures of Adult Prairie Voles are Correlated with Residency Status and Genetic Parentage

Examination of extensive data from field and laboratory studies indicates that prairie voles (Microtus ochrogaster) are socially monogamous and form pair-bonds. We used grid-trapping data from replicate populations of prairie voles living in 0.1-ha small mammal enclosures at 2 different initial densities to examine the extent to which opposite-sex adults captured together in the same live trap reflected social associations established from nest-use patterns and the probability that the pair produced offspring. Females classified as a resident at a nest that also included at least 1 resident male (male–female pairs or groups) were significantly more likely to be trapped with a male from the same social unit (64%) rather than a male from another social unit or a male wanderer (an animal not considered a resident at any nest site). On the other hand, females residing at a nest with no resident males were caught with wandering males significantly more often (84%) than with resident males from another nest. Finally, female wanderers were significantly more likely to be trapped with male wanderers (75%) than with resident males. A genetic analysis of parentage revealed that females were significantly more likely to have produced offspring with the male with which they were caught most frequently (80% of females) than to not breed with these males. None of these findings were influenced by density. Overall, the multiple-capture data were consistent with social monogamy and the relative frequency of male–female multiple captures were predictive of the likelihood of mating. However, although most females residing at nests with resident males bred with these males (84%), a similar percentage of these females also bred with at least 1 male that never resided in the same social unit as the female, suggesting that prairie voles are not genetically monogamous throughout their lives.

Estimates of reproductive success for group-living prairie voles, Microtus ochrogaster, in high-density populations

Examination of the reproductive success of cooperative breeders can provide insights into costs and benefits of group living. We tested two hypotheses proposed to account for group living in prairie voles. One hypothesis suggests that ecological constraints such as the lack of available territories may cause delayed dispersal leading to formation of groups. The other hypothesis suggests that benefits of group living outweigh the benefits of dispersal. If the benefits of group living outweigh the costs, then per capita reproductive success should increase with increasing group size. If ecological constraints prevent dispersal, then lifetime reproductive success may not differ in groups of different sizes, or there may be an inverse relationship between per capita lifetime reproductive success and group size. We also investigated whether food supplementation (higher-quality habitat) and the number of breeding females per group influenced lifetime reproductive success. During two summers, we monitored reproductive success of food-supplemented and unsupplemented populations of prairie voles in 0.1 ha enclosures. Live trapping allowed us to identify residents of breeding units. We found that per capita reproductive success increased with group size in food-supplemented populations. This result was not due to the presence of additional breeding females since per capita production of offspring decreased in groups with larger numbers of breeding females. Thus, larger groups may benefit the breeding female, but the presence of additional breeding females per group appears costly.

Demography of fluctuating prairie vole populations: comparison of demographic variables among phases of fluctuations

We tested for differences in the proportion of reproductively active males and females, proportion of the population composed of young and immigrants, and monthly survival (total, adult, young) among phases (trough, increase, and decline) and among habitats (alfalfa, bluegrass, and tallgrass) of 30 population fluctuations ofMicrotus ochrogaster Wagner, 1842 over 25 years in east-central Illinois USA. Total population survival and survival of adults and young were greatest during the increase phase, among fluctuations, irrespective of habitat. The proportion of reproductively active adult males and females was lowest during the decline phase, an effect of lower reproduction during the winter. These results suggest that phase-specific changes in survival were the primary demographic factor driving population fluctuations ofM. ochrogaster in our study sites. We conclude that small-scale spatially different population fluctuations may be explained by the same mechanisms that explain fluctuations within a population.

Morphological, Genetic, and Behavioral Comparisons of Two Prairie Vole Populations in the Field and Laboratory

Reports of geographic variation in behavior and morphology among prairie voles (Microtus ochrogaster) from Illinois, Kansas, and Tennessee have led to the belief that these animals vary in their mating strategies and the degree to which they are monogamous. Despite this, few studies have directly compared behavior between populations. Because the prairie vole is commonly discussed as a model for mammalian monogamy, understanding how aspects of social attachment and the mating system vary could provide further insight into the evolution of monogamy. We therefore conducted a series of experiments in the laboratory and field to assess morphological, behavioral, or genetic differences between 2 populations of this species. Voles from Illinois were morphologically similar to voles from Tennessee and exhibited comparable social and mating behavior under both laboratory and field conditions. Although genetically distinct, the 2 populations demonstrated similar levels of heterozygosity and allelic richness. Sexual dimorphism, a common indicator of mating strategy, was absent in voles from 7 widely distributed regions from across their geographic range. In the context of these results, we question the degree to which the previously described population differences are ecologically meaningful. If differences between prairie voles from Kansas and Illinois do indeed exist, examination of our data suggests that those from Kansas are atypical of prairie voles overall.

Parental regulation of central patterns of estrogen receptor α

Reduced levels of estrogen receptor alpha (ERα) in the medial amygdala (MeA) and bed nucleus of stria terminalis (BST) have been hypothesized to play a significant role in the expression of male behaviors associated with monogamy. Therefore, the regulation of ERα could be a critical factor in determining male behavior and the evolution of monogamy. Central expression of ERα immunoreactivity was compared in hybrid offspring from crosses between two phenotypically distinct populations of prairie voles ( Microtus ochrogaster). Illinois voles (IL) are socially monogamous and display low levels of ERα, while Kansas voles (KN) display some characteristics associated with polygyny and have higher levels of ERα. In offspring from hybrid crosses, the pattern of ERα expression was dependent upon parentage; the two types of hybrid crosses did not produce the same ERα pattern in the offspring. In the BST and MeA, hybrid males expressed ERα patterns consistent with those of males from their mother’s population, while hybrid females had ERα patterns typical of females belonging to their father’s population. The parental-specific patterns of ERα expression are suggestive of genomic imprinting, therefore, the vole ERα ( Esr1) gene was cloned and sequenced, and examined for allele-specific expression. Results from this study indicate that while maternal factors may play a major role the expression of ERα in their male offspring, genomic imprinting is unlikely to be involved, suggesting another mechanism is responsible.

Environmental stochasticity: empirical estimates of prairie vole survival with implications for demographic models

A rich theory exists regarding the potential impact of correlations among vital rates on population projections derived from demographic models. However, relatively little is known about the magnitude of correlations among vital rates in natural populations, particularly in mammals. We used 30 years of mark–recapture data from a population of prairie voles ( Microtus ochrogaster (Wagner, 1842)) to test for differences in survival among mass classes and sexes, in correlations among vital rates, in correlations between vital rates and environmental factors, and in autocorrelation in vital rates. Estimated monthly survival rates did not differ significantly among mass classes and there were no significant cross-correlations among mass classes. Survival of large prairie voles increased in mild winters (i.e., warm temperatures and low snowfall). Survival rates of medium and large voles were negatively autocorrelated at time lags of 9–12 months, and survivals of large voles were positively autocorrelated for time lags of <3 months. These autocorrelations were not explained by patterns of temperature or precipitation. The observed degree of autocorrelation in vital rates is sufficient to affect projections from demographic models, particularly in short-lived taxa that require seasonal or monthly estimation of vital rates.

The effect of habitat size and predation on the time to extinction of prairie vole populations: simulation studies via SERDYCA

We present a spatially explicit individual-based model of rodent dynamics, customized for the prairie vole species, Microtus ochrogaster. The model strives to represent the complexity of intertwining factors that determine the spatio-temporal dynamics of small rodents. It is based on trophic relationships and incorporates important features such as territorial competition, mating behavior, density-dependent predation and dispersal out of the modeled spatial region. Vegetation growth and vole fecundity are dependent on climatic components. The results of simulations show that the model correctly predicts the overall temporal dynamics of the population density. Time-series analysis shows a very good match between the periods corresponding to the peak population density frequencies predicted by the model and the ones reported in the literature. The model is used to study the relation between persistence, landscape area and predation. We use the notions of average time to extinction (ATE) and persistence frequency to quantify persistence. While the ATE decreases with decrease of area, it is a bell-shaped function of the predation level: increasing for “small” and decreasing for “large” predation levels.

EFFECTS OF FEMALE IMMIGRANTS ON DEMOGRAPHY AND SOCIAL ORGANIZATION OF PRAIRIE VOLE (MICROTUS OCHROGASTER) POPULATIONS

We experimentally investigated effects of female immigrants on demography and social organization of prairie vole (Microtus ochrogaster) populations. We tested the hypothesis that increased immigrant pressure by unrelated adult females would decrease the survivorship of juveniles and indirectly decrease the proportion of communal groups in the populations. We established prairie vole populations in 8 enclosures (32 × 32 m). Four populations were supplemented with adult female immigrants, and the other 4 served as control populations in which no females were introduced. The results showed that adult female immigrants reduced the proportion of females and the proportion of juveniles in resident populations but did not change the social organization. We concluded that adult female immigrants did negatively affect resident populations. However, the direct numerical input and subsequent reproduction by immigrants would compensate for their negative effect on resident populations.